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A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs.

Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA - J. Cell Biol. (2005)

Bottom Line: Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu.We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex.We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Michael Hooker Microscopy Facility, University of North Carolina School of Medicine, Chapel Hill, NC 27599, USA. patrick_vincent@med.unc.edu

ABSTRACT
Phosphatidylinositol (PtdIns) transfer proteins (PITPs) regulate signaling interfaces between lipid metabolism and membrane trafficking. Herein, we demonstrate that AtSfh1p, a member of a large and uncharacterized Arabidopsis thaliana Sec14p-nodulin domain family, is a PITP that regulates a specific stage in root hair development. AtSfh1p localizes along the root hair plasma membrane and is enriched in discrete plasma membrane domains and in the root hair tip cytoplasm. This localization pattern recapitulates that visualized for PtdIns(4,5)P2 in developing root hairs. Gene ablation experiments show AtSfh1p izygosity compromises polarized root hair expansion in a manner that coincides with loss of tip-directed PtdIns(4,5)P2, dispersal of secretory vesicles from the tip cytoplasm, loss of the tip f-actin network, and manifest disorganization of the root hair microtubule cytoskeleton. Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu. We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex. We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

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The A. thaliana Sec14p-nodulin domain family. (A) Schematic alignment of Sec14p with AtSFH gene products (identified by TAIR accession numbers). Primary sequence identities/homologies with Sec14p are indicated. Probabilities that these relationships are random are given (E-values). The indicated K66, E207, and K239 residues critical for Sec14p binding of phosphatidylinositol are highly conserved (Phillips et al., 1999). (B) Primary sequence alignment of the COOH-terminal 70 AtSFH nodulin domain residues with those of the Nlj16 nodulin (Szczyglowski et al., 1997). Conserved identities and similarities are highlighted. Schematic illustration of the domain organization of four members of this family from the legume Lotus japonicus is also shown. These LjPLPs exhibit COOH-terminal Nlj16 nodulin domains.
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fig1: The A. thaliana Sec14p-nodulin domain family. (A) Schematic alignment of Sec14p with AtSFH gene products (identified by TAIR accession numbers). Primary sequence identities/homologies with Sec14p are indicated. Probabilities that these relationships are random are given (E-values). The indicated K66, E207, and K239 residues critical for Sec14p binding of phosphatidylinositol are highly conserved (Phillips et al., 1999). (B) Primary sequence alignment of the COOH-terminal 70 AtSFH nodulin domain residues with those of the Nlj16 nodulin (Szczyglowski et al., 1997). Conserved identities and similarities are highlighted. Schematic illustration of the domain organization of four members of this family from the legume Lotus japonicus is also shown. These LjPLPs exhibit COOH-terminal Nlj16 nodulin domains.

Mentions: A search of the National Center for Biotechnology Information and The Arabidopsis Information Resource databases identified 31 homologous A. thaliana sequences when the Sec14p primary sequence was queried. These sequences each exhibit a 239-residue domain that shares significant primary sequence homology with the Sec14p lipid binding domain (LBD), and these domains fall into two Sec14p homology groups. One Sec14p homology group encodes proteins that consist of a Sec14p domain that shares rather low (but significant) sequence identity with yeast Sec14p. The other Sec14p homology group consists of the 14 highest-scoring Sec14p LBD-like sequences. 11 of these 14 sequences represent proteins where an NH2-terminal Sec14p domain is joined to a COOH-terminal nodulin domain of ∼100 residues (Fig. 1 A). These nodulin domains define three classes based on similarity to the Nlj16 nodulin (Fig. 1 B). Nlj16 is expressed by root cells of the legume Lotus japonicus upon infection with Rhizobium and defines a plasma membrane targeting module (Kapranov et al., 2001). Lotus expresses four Sec14p-nodulin domain genes (LjPLP-I thru LjPLP-IV; Fig. 1 B). The Sec14p-nodulin domain proteins are of special interest because of the unanticipated physical linkage of Sec14p and nodulin domains, and because these define unique examples of membrane-bound Sec14p-like PITPs.


A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs.

Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA - J. Cell Biol. (2005)

The A. thaliana Sec14p-nodulin domain family. (A) Schematic alignment of Sec14p with AtSFH gene products (identified by TAIR accession numbers). Primary sequence identities/homologies with Sec14p are indicated. Probabilities that these relationships are random are given (E-values). The indicated K66, E207, and K239 residues critical for Sec14p binding of phosphatidylinositol are highly conserved (Phillips et al., 1999). (B) Primary sequence alignment of the COOH-terminal 70 AtSFH nodulin domain residues with those of the Nlj16 nodulin (Szczyglowski et al., 1997). Conserved identities and similarities are highlighted. Schematic illustration of the domain organization of four members of this family from the legume Lotus japonicus is also shown. These LjPLPs exhibit COOH-terminal Nlj16 nodulin domains.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2171805&req=5

fig1: The A. thaliana Sec14p-nodulin domain family. (A) Schematic alignment of Sec14p with AtSFH gene products (identified by TAIR accession numbers). Primary sequence identities/homologies with Sec14p are indicated. Probabilities that these relationships are random are given (E-values). The indicated K66, E207, and K239 residues critical for Sec14p binding of phosphatidylinositol are highly conserved (Phillips et al., 1999). (B) Primary sequence alignment of the COOH-terminal 70 AtSFH nodulin domain residues with those of the Nlj16 nodulin (Szczyglowski et al., 1997). Conserved identities and similarities are highlighted. Schematic illustration of the domain organization of four members of this family from the legume Lotus japonicus is also shown. These LjPLPs exhibit COOH-terminal Nlj16 nodulin domains.
Mentions: A search of the National Center for Biotechnology Information and The Arabidopsis Information Resource databases identified 31 homologous A. thaliana sequences when the Sec14p primary sequence was queried. These sequences each exhibit a 239-residue domain that shares significant primary sequence homology with the Sec14p lipid binding domain (LBD), and these domains fall into two Sec14p homology groups. One Sec14p homology group encodes proteins that consist of a Sec14p domain that shares rather low (but significant) sequence identity with yeast Sec14p. The other Sec14p homology group consists of the 14 highest-scoring Sec14p LBD-like sequences. 11 of these 14 sequences represent proteins where an NH2-terminal Sec14p domain is joined to a COOH-terminal nodulin domain of ∼100 residues (Fig. 1 A). These nodulin domains define three classes based on similarity to the Nlj16 nodulin (Fig. 1 B). Nlj16 is expressed by root cells of the legume Lotus japonicus upon infection with Rhizobium and defines a plasma membrane targeting module (Kapranov et al., 2001). Lotus expresses four Sec14p-nodulin domain genes (LjPLP-I thru LjPLP-IV; Fig. 1 B). The Sec14p-nodulin domain proteins are of special interest because of the unanticipated physical linkage of Sec14p and nodulin domains, and because these define unique examples of membrane-bound Sec14p-like PITPs.

Bottom Line: Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu.We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex.We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Michael Hooker Microscopy Facility, University of North Carolina School of Medicine, Chapel Hill, NC 27599, USA. patrick_vincent@med.unc.edu

ABSTRACT
Phosphatidylinositol (PtdIns) transfer proteins (PITPs) regulate signaling interfaces between lipid metabolism and membrane trafficking. Herein, we demonstrate that AtSfh1p, a member of a large and uncharacterized Arabidopsis thaliana Sec14p-nodulin domain family, is a PITP that regulates a specific stage in root hair development. AtSfh1p localizes along the root hair plasma membrane and is enriched in discrete plasma membrane domains and in the root hair tip cytoplasm. This localization pattern recapitulates that visualized for PtdIns(4,5)P2 in developing root hairs. Gene ablation experiments show AtSfh1p izygosity compromises polarized root hair expansion in a manner that coincides with loss of tip-directed PtdIns(4,5)P2, dispersal of secretory vesicles from the tip cytoplasm, loss of the tip f-actin network, and manifest disorganization of the root hair microtubule cytoskeleton. Derangement of tip-directed Ca2+ gradients is also apparent and results from isotropic influx of Ca2+ from the extracellular milieu. We propose AtSfh1p regulates intracellular and plasma membrane phosphoinositide polarity landmarks that focus membrane trafficking, Ca2+ signaling, and cytoskeleton functions to the growing root hair apex. We further suggest that Sec14p-nodulin domain proteins represent a family of regulators of polarized membrane growth in plants.

Show MeSH
Related in: MedlinePlus